Arthropod eyes: The early Cambrian fossil record and divergent evolution of visual systems. Issue 2 (March 2016)

• Record Type: Journal Article
• Authors: Strausfeld, Nicholas J.; Ma, Xiaoya; Edgecombe, Gregory D.; Fortey, Richard A.; Land, Michael F.; Liu, Yu; Cong, Peiyun; Hou, Xianguang
• Is Part Of: Arthropod structure & development. Volume 45:Issue 2(2016:Mar.)
• Page Start: 152
• Page End: 172
• Publication Date: 2016-03
• Subjects: Apposition eyes -- Optic lobes -- Ground pattern organization -- Divergent evolution -- Radiodonta -- Euarthropoda; Arthropoda -- Morphology -- Periodicals; Arthropoda -- Anatomy -- Periodicals; Arthropoda -- Cytology -- Periodicals; Arthropods -- growth & development -- Periodicals; 595
• DOI: 10.1016/j.asd.2015.07.005
• Languages: English
• ISSNs: 1467-8039

Abstract

Abstract: Four types of eyes serve the visual neuropils of extant arthropods: compound retinas composed of adjacent facets; a visual surface populated by spaced eyelets; a smooth transparent cuticle providing inwardly directed lens cylinders; and single-lens eyes. The first type is a characteristic of pancrustaceans, the eyes of which comprise lenses arranged as hexagonal or rectilinear arrays, each lens crowning 8–9 photoreceptor neurons. Except for Scutigeromorpha, the second type typifies Myriapoda whose relatively large eyelets surmount numerous photoreceptive rhabdoms stacked together as tiers. Scutigeromorph eyes are facetted, each lens crowning some dozen photoreceptor neurons of a modified apposition-type eye. Extant chelicerate eyes are single-lensed except in xiphosurans, whose lateral eyes comprise a cuticle with a smooth outer surface and an inner one providing regular arrays of lens cylinders. This account discusses whether these disparate eye types speak for or against divergence from one ancestral eye type. Previous considerations of eye evolution, focusing on the eyes of trilobites and on facet proliferation in xiphosurans and myriapods, have proposed that the mode of development of eyes in those taxa is distinct from that of pancrustaceans and is the plesiomorphic condition from which facetted eyes have evolved. But the recent discovery of enormous regularly facetted compound eyes belonging to early Cambrian radiodontans suggests that high-resolution facetted eyes with superior optics may be the ground pattern organization for arthropods, predating the evolution of arthrodization and jointed post-protocerebral appendages. Here we provide evidence that compound eye organization in stem-group euarthropods of the Cambrian can be understood in terms of eye morphologies diverging from this ancestral radiodontan-type ground pattern. We show that in certain Cambrian groups apposition eyes relate to fixed or mobile eyestalks, whereas other groups reveal concomitant evolution of sessile eyes equipped with optics typical of extant xiphosurans. Observations of fossil material, including that of trilobites and eurypterids, support the proposition that the ancestral compound eye was the apposition type. Cambrian arthropods include possible precursors of mandibulate eyes. The latter are the modified compound eyes, now sessile, and their underlying optic lobes exemplified by scutigeromorph chilopods, and the mobile stalked compound eyes and more elaborate optic lobes typifying Pancrustacea. Radical divergence from an ancestral apposition type is demonstrated by the evolution of chelicerate eyes, from doublet sessile-eyed stem-group taxa to special apposition eyes of xiphosurans, the compound eyes of eurypterids, and single-lens eyes of arachnids. Different eye types are discussed with respect to possible modes of life of the extinct species that possessed them, comparing these to extant counterparts and the types of visual centers the eyes might have served. Highlights: Exceptionally preserved lower Cambrian arthropods resolve eye morphologies and preserved traces of brain and optic lobes. Evidence is provided that supports apposition optics as the ancestral eye type, typified by the compound eyes of Radiodonta. Evolved modifications account for divergent evolution of Limulus -type compound eyes and chelicerate single lens eyes. Eyes of Trilobita, Myriapoda and Insecta relate to evolved modifications of the plesiomorphic apposition compound eye. Visual systems defined by nested optic neuropils are distinct from channels associated with median ocelli and nauplius eyes.